A novel atherothrombotic model of ischemic stroke induced by injection of collagen into the cerebral vasculature

Journal of Neuroscience Methods

Volumn 239, Issue , 2015, Pages 65-74

  Schunke, Kathryn J ^a   Toung, Thomas K ^a   Zhang, Jian ^a   Pathak, Arvind P ^a   Xu, Jiadi ^b   Zhang, Jiangyang ^a   Koehler, Raymond C ^a   Faraday, Nauder ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

Atherothrombosis; Collagen; Ischemic stroke; Mouse; Platelet; Rat

Indexed keywords

COLLAGEN; FIBRIN; FIBRINOGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; BLOOD CLOTTING; BLOOD VESSEL OCCLUSION; BRAIN ARTERY; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN CIRCULATION; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PERFUSION; COGNITIVE DEFECT; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ECHO PLANAR IMAGING; EXPERIMENTAL THROMBOSIS; IMMUNOFLUORESCENCE MICROSCOPY; INTERNAL CAROTID ARTERY; LASER DOPPLER FLOWMETRY; LOCOMOTION; MALE; MICRO-COMPUTED TOMOGRAPHY; MIDDLE CEREBRAL ARTERY; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; RAT; RESPIRATORY GATED IMAGING; THROMBOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COMPLICATION; COMPUTER ASSISTED TOMOGRAPHY; DISEASE MODEL; DRUG EFFECTS; HEMISPHERIC DOMINANCE; NERVOUS SYSTEM DISEASES; NEUTROPHIL; NONPARAMETRIC TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; STROKE; TIME FACTOR; WISTAR RAT;

ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; COLLAGEN; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; LASER-DOPPLER FLOWMETRY; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; NERVOUS SYSTEM DISEASES; NEUTROPHILS; RATS; RATS, WISTAR; STATISTICS, NONPARAMETRIC; STROKE; TIME FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84908342459     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2014.10.001     Document Type: Article

References (39)

1. Alkayed N.J., Harukuni I., Kimes A.S., London E.D., Traystman R.J., Hurn P.D. Gender-linked brain injury in experimental stroke. Stroke 1998, 29:159-165. [discussion 166].
2. Badimon L., Vilahur G. Platelets, arterial thrombosis and cerebral ischemia. Cerebrovasc Dis 2007, 24(Suppl. 1):30-39.
3. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994, 103:247-254.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 1996, 111:209-219.
5. Bederson J.B., Pitts L.H., Tsuji M., Nishimura M.C., Davis R.L., Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986, 17:472-476.
6. Cebulla J., Kim E., Rhie K., Zhang J., Pathak A.P. Multiscale and multi-modality visualization of angiogenesis in a human breast cancer model. Angiogenesis 2014, 17(3):695-709.
7. Davi G., Patrono C. Platelet activation and atherothrombosis. N Engl J Med 2007, 357:2482-2494.
8. Duhamel G., Callot V., Tachrount M., Alsop D.C., Cozzone P.J. Pseudo-continuous arterial spin labeling at very high magnetic field (11.75T) for high-resolution mouse brain perfusion imaging. Magn Reson Med 2012, 67:1225-1236.
9. Eliasson M.J., Sampei K., Mandir A.S., Hurn P.D., Traystman R.J., Bao J., et al. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 1997, 3:1089-1095.
10. Faraday N., Braunstein J.B., Heldman A.W., Bolton E.D., Chiles K.A., Gerstenblith G., et al. Prospective evaluation of the relationship between platelet-leukocyte conjugate formation and recurrent myocardial ischemia in patients with acute coronary syndromes. Platelets 2004, 15:9-14.
11. Faraday N., Schunke K., Saleem S., Fu J., Wang B., Zhang J., et al. Cathepsin G-dependent modulation of platelet thrombus formation in vivo by blood neutrophils. PLoS ONE 2013, 8:e71447.
12. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
13. Fuster V., Stein B., Ambrose J.A., Badimon L., Badimon J.J., Chesebro J.H. Atherosclerotic plaque rupture and thrombosis. Evolving concepts. Circulation 1990, 82:II47-II59.
14. Hennerici M.G. The unstable plaque. Cerebrovasc Dis 2004, 17(Suppl. 3):17-22.
15. Hossmann K.A. The two pathophysiologies of focal brain ischemia: implications for translational stroke research. J Cereb Blood Flow Metab 2012, 32:1310-1316.
16. Ishikawa T., Shimizu M., Kohara S., Takizawa S., Kitagawa Y., Takagi S. Appearance of WBC-platelet complex in acute ischemic stroke, predominantly in atherothrombotic infarction. J Atheroscler Thromb 2012, 19:494-501.
17. Kleinschnitz C., Braeuninger S., Pham M., Austinat M., Nolte I., Renne T., et al. Blocking of platelets or intrinsic coagulation pathway-driven thrombosis does not prevent cerebral infarctions induced by photothrombosis. Stroke 2008, 39:1262-1268.
18. Lansberg M.G., O'Donnell M.J., Khatri P., Lang E.S., Nguyen-Huynh M.N., Schwartz N.E., et al. Antithrombotic and thrombolytic therapy for ischemic stroke: antithrombotic therapy and prevention of thrombosis, 9th ed: American college of chest physicians evidence-based clinical practice guidelines. Chest 2012, 141:e601S-e636S. American College of Chest Physicians.
19. Lin T.N., He Y.Y., Wu G., Khan M., Hsu C.Y. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 1993, 24:117-121.
20. Lovett J.K., Coull A.J., Rothwell P.M. Early risk of recurrence by subtype of ischemic stroke in population-based incidence studies. Neurology 2004, 62:569-573.
21. Macrae I.M. Preclinical stroke research - advantages and disadvantages of the most common rodent models of focal ischaemia. Br J Pharmacol 2011, 164:1062-1078.
22. Marinescu M., Bouley J., Chueh J., Fisher M., Henninger N. Clot injection technique affects thrombolytic efficacy in a rat embolic stroke model: implications for translaboratory collaborations. J Cereb Blood Flow Metab 2014, 34:677-682.
23. Marnane M., Prendeville S., McDonnell C., Noone I., Barry M., Crowe M., et al. Plaque inflammation and unstable morphology are associated with early stroke recurrence in symptomatic carotid stenosis. Stroke 2014, 45:801-806.
24. Michelson A.D., Barnard M.R., Krueger L.A., Valeri C.R., Furman M.I. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001, 104:1533-1537.
25. Murray C.J., Lopez A.D. Measuring the global burden of disease. N Engl J Med 2013, 369:448-457.
26. Nieswandt B., Pleines I., Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J Thromb Haemost 2011, 9(Suppl. 1):92-104.
27. Orset C., Macrez R., Young A.R., Panthou D., Angles-Cano E., Maubert E., et al. Mouse model of in situ thromboembolic stroke and reperfusion. Stroke 2007, 38:2771-2778.
28. Papangelou A., Toung T.J., Gottschalk A., Mirski M.A., Koehler R.C. Infarct volume after hyperacute infusion of hypertonic saline in a rat model of acute embolic stroke. Neurocrit Care 2013, 18:106-114.
29. Pathak A.P., Kim E., Zhang J., Jones M.V. Three-dimensional imaging of the mouse neurovasculature with magnetic resonance microscopy. PLoS ONE 2011, 6:e22643.
30. Peters J.M., Maclean A.V., Young G.S. Rapid resolution of diffusion weighted MRI abnormality in a patient with a stuttering stroke. BMJ Case Rep 2010, 2010. [Epub 2010 February 8]. 10.1136/bcr.07.2009.2063.
31. Redgrave J.N., Lovett J.K., Gallagher P.J., Rothwell P.M. Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford plaque study. Circulation 2006, 113:2320-2328.
32. Roger V.L., Go A.S., Lloyd-Jones D.M., Benjamin E.J., Berry J.D., Borden W.B., et al. Heart disease and stroke statistics - 2012 update: a report from the American Heart Association. Circulation 2012, 125:e2-e220. American Heart Association Statistics Committee and Stroke Statistics Subcommittee.
33. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., Sharp F.R. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 1990, 10:290-293.
34. Takahashi H., Kirsch J.R., Hashimoto K., London E.D., Koehler R.C., Traystman R.J. PPBP [4-phenyl-1-(4-phenylbutyl) piperidine] decreases brain injury after transient focal ischemia in rats. Stroke 1996, 27:2120-2123.
35. Tanabe J.L., Yongbi M., Branch C., Hrabe J., Johnson G., Helpern J.A. MR perfusion imaging in human brain using the UNFAIR technique. Un-inverted flow-sensitive alternating inversion recovery. J Magn Reson Imaging 1999, 9:761-767.
36. Warden B.A., Willman A.M., Williams C.D. Antithrombotics for secondary prevention of noncardioembolic ischaemic stroke. Nat Rev Neurol 2012, 8:223-235.
37. Wu D., Xu J., McMahon M.T., van Zijl P.C., Mori S., Northington F.J., et al. In vivo high-resolution diffusion tensor imaging of the mouse brain. Neuroimage 2013, 83:18-26.
38. Zhang R.L., Chopp M., Zhang Z.G., Jiang Q., Ewing J.R. A rat model of focal embolic cerebral ischemia. Brain Res 1997, 766:83-92.
39. Zhang Z.G., Zhang L., Tsang W., Goussev A., Powers C., Ho K.L., et al. Dynamic platelet accumulation at the site of the occluded middle cerebral artery and in downstream microvessels is associated with loss of microvascular integrity after embolic middle cerebral artery occlusion. Brain Res 2001, 912:181-194.